Ultrastructural heterogeneity of spinal terminations in the cat inferior olive

Abstract

Three different functional regions of the inferior olive receive direct input from the spinal cord. The present study examined spinal termination patterns in two of these functional entities, the rostral and caudal halves of the dorsal accessory olive, with anterograde transport of wheat germ agglutinin conjugated with horseradish peroxidase visualized by tetramethylbenzidine. The injections primarily included the spino-olivary projection from neurons in the lumbosacral dorsal horn. Two types of labeled terminals were found, small end bulbs (84%) and large en passant boutons (16%). The small end bulbs displayed distinct rostrocaudal variations in their termination patterns. In the rostral dorsal accessory olive they synapsed most frequently on dendrites that directly contacted other dendrites, forming dendritic thickets. In the caudal dorsal accessory olive, they synapsed less often in thickets and more often on isolated dendrites. Conversely, the large, en passant boutons synapsed primarily in thickets and failed to display comparable rostrocaudal shifts. All somatic afferents in the rostral dorsal accessory olive examined to date synapse primarily in dendritic thickets, suggesting that the thicket is a major site through which neurons in that region detect peripheral somatic events. Within dendritic thickets, single afferents often contact multiple dendrites and the dendrites, in turn, sometimes give rise to spinous processes. It is proposed that these spinous processes participate in synaptic glomeruli. which others have shown to be the primary targets of cerebellar afferents to the dorsal accessory olive. These results suggest that somatic afferents to the rostral dorsal accessory olive influence a greater number of neurons and are more likely to interact with cerebellar input than are somatic afferents to the caudal region. This possibility is consistent with the more complex types of movement influenced by the rostral compared with the caudal halves of the dorsal accessory olive.